Caenorhabditis elegans sperm carry a histone-based epigenetic memory of both spermatogenesis and oogenesis

Tomoko M Tabuchi,Tess E Jeffers,Andreas Rechtsteiner,Thea A Egelhofer,Susan Strome,Coleen T Murphy

doi:10.1038/s41467-018-06236-8

Tomoko M Tabuchi, Tess E Jeffers + Show 4 more

Open Access

https://doi.org/10.1038/s41467-018-06236-8

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Abstract

Paternal contributions to epigenetic inheritance are not well understood. Paternal contributions via marked nucleosomes are particularly understudied, in part because sperm in some organisms replace the majority of nucleosome packaging with protamine packaging. Here we report that in Caenorhabditis elegans sperm, the genome is packaged in nucleosomes and carries a histone-based epigenetic memory of genes expressed during spermatogenesis, which unexpectedly include genes well known for their expression during oogenesis. In sperm, genes with spermatogenesis-restricted expression are uniquely marked with both active and repressive marks, which may reflect a sperm-specific chromatin signature. We further demonstrate that epigenetic information provided by sperm is important and in fact sufficient to guide proper germ cell development in offspring. This study establishes one mode of paternal epigenetic inheritance and offers a potential mechanism for how the life experiences of fathers may impact the development and health of their descendants.

Highlights

Paternal contributions to epigenetic inheritance are not well understood
C. elegans sperm retain at least some histone packaging of the genome[9,10,11], deliver chromosomes marked with histone modifications to embryos[9,10,11], and can transmit a chromatinbased memory of temperature, diet, and stress to offspring[12,13,14]
We focused on a modification associated with gene repression and two modifications associated with gene expression (H3K36me[3] and H3K4me3), because these modifications have been implicated in transgenerational epigenetic inheritance in C. elegans[9,11,14,15,16,17,18]

Summary

Introduction

Paternal contributions to epigenetic inheritance are not well understood. Paternal contributions via marked nucleosomes are understudied, in part because sperm in some organisms replace the majority of nucleosome packaging with protamine packaging. C. elegans sperm retain at least some histone packaging of the genome[9,10,11], deliver chromosomes marked with histone modifications to embryos[9,10,11], and can transmit a chromatinbased memory of temperature, diet, and stress to offspring[12,13,14]. We document that C. elegans sperm retain modified histones genomewide, similar to zebrafish sperm, and that sperm carry a histone-based epigenetic memory of genes with spermatogenesis-restricted expression and unexpectedly genes with oogenesis-enriched expression. Our studies establish modified histones retained in mature sperm as one mechanism by which fathers may transmit heritable traits, and highlight a role for sperm epigenetics in the development and fertility of descendants

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